Skip to main content

Advertisement

Log in

Malacosporean-like spores in urine of rainbow trout react with antibody and DNA probes to Tetracapsuloides bryosalmonae

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Tetracapsuloides bryosalmonae is the myxozoan parasite causing proliferative kidney disease (PKD) of salmonid fishes in Europe and North America. The complete life cycle of the parasite remains unknown despite recent discoveries that the stages infectious for fish develop in freshwater bryozoans. During the course of examinations of the urine of rainbow trout (Oncorhynchus mykiss) with or recovering from PKD we identified spores with features similar to those of T. bryosalmonae found in the bryozoan host. Spores found in the urine were subspherical, with a width of 16 µm and height of 14 µm, and possessed two soft valves surrounding two spherical polar capsules (2 µm in diameter) and a single sporoplasm. The absence of hardened valves is a distinguishing characteristic of the newly established class Malacosporea that includes T. bryosalmonae as found in the bryozoan host. The parasite in the urine of rainbow trout possessed only two polar capsules and two valve cells compared to the four polar capsules and four valves observed in the spherical spores of 19 µm in diameter from T. bryosalmonae from the bryozoan host. Despite morphological differences, a relationship between the spores in the urine of rainbow trout and T. bryosalmonae was demonstrated by binding of monoclonal and polyclonal antibodies and DNA probes specific to T. bryosalmonae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Anderson CL, Canning EU, Okamura B (1999a) 18S rDNA sequences indicate that PKX organism parasitizes Bryozoa. Bull Eur Assoc Fish Pathol 19:94–97

    Google Scholar 

  • Anderson CL, Canning EU, Okamura B (1999b) Molecular data implicate bryozoans as hosts for PKX (Phylum Myxozoa) and identify a clade of bryozoan parasites within the Myxozoa. Parasitology 119:555–561

    Article  PubMed  Google Scholar 

  • Antonio DB, Andree KB, McDowell TS, Hedrick RP (1998) Detection of Myxobolus cerebralis in rainbow trout and oligochaete tissues by using a nonradioactive in situ hybridization (ISH) protocol. J Aquat Anim Health 10:338–347

    Google Scholar 

  • Black CM (2000) Collection of body fluids. In: Ostrander GK (ed) The laboratory fish. Academic, San Diego, pp 513–521

  • Canning EU, Okamura B, Curry A (1996) Development of a myxozoan parasite Tetracapsula bryozoides gen. n. sp. n. in Cristatella mucedo ( Bryozoa: Phylactolaemata). Folia Parasitol 43:249–261

    Google Scholar 

  • Canning EU, Curry A, Feist SW, Longshaw M, Okamura B (1999) Tetracapsula bryosalmonae n. sp. for PKX organism, the cause of PKD in salmonid fish. Bull Eur Assoc Fish Pathol 19:203–206

    Google Scholar 

  • Canning EU, Curry A, Feist SW, Longshaw M, Okamura B (2000) A new class and order of myxozoans to accommodate parasites of bryozoans with ultrastructural observations on Tetracapsula bryosalmonae (PKX organism). J Eukaryot Microbiol 47:456–468

    CAS  PubMed  Google Scholar 

  • Canning EU, Tops S, Curry A, Wood TS, Okamura B (2002) Ecology, development, and pathogenicity of Buddenbrockia plumatellae Schroder 1910 (Myxozoa, Malacospora) (syn. Tetracapsula bryozoides) and establishment of Tetracapsuloides n. gen. for Tetracapsula bryosalmonae. J Eukaryot Microbiol 49:280–295

    PubMed  Google Scholar 

  • Chilmonczyk S, Monge D, De Kinkelin P (2002) Proliferative kidney disease: cellular aspects of the rainbow trout, Oncorhynchus mykiss (Walbaum), response to parasitic infection. J Fish Dis 25:217–226

    Article  Google Scholar 

  • Clifton-Hadley RS, Feist SW (1989) Proliferative kidney disease in brown trout Salmo trutta: further evidence of a myxosporean aetiology. Dis Aquat Org 6:99–103

    Google Scholar 

  • El-Matbouli M, Holstein TW, Hoffmann RW (1998) Determination of nuclear DNA concentration in cells of Myxobolus cerebralis and triactinomyxon spores, the causative agent of whirling disease. Parasitol Res 84:694–699

    Article  CAS  PubMed  Google Scholar 

  • Feist SW, Bucke D (1993) Proliferative kidney disease in wild salmonids. Fish Res 3:277–290

    Google Scholar 

  • Feist SW, Longshaw M, Canning EU, Okamura B (2001) Induction of proliferative kidney disease (PKD) in rainbow trout Oncorhynchus mykiss via the bryozoan Fredericella sultana infected with Tetracapsula bryosalmonae. Dis Aquat Org 45:61–68

    CAS  PubMed  Google Scholar 

  • Ferguson HW, Needham EA (1978) Proliferative kidney disease in rainbow trout Salmo gairdneri Richardson. J Fish Dis 1:91–108

    Google Scholar 

  • Foott JS, Hedrick RP (1987) Seasonal occurrence of the infectious stage of proliferative kidney disease (PKD) and resistance of rainbow trout, Salmo gairdneri Richardson, to reinfection. J Fish Biol 30:477–483

    Google Scholar 

  • Hedrick RP, Kent ML, Toth RJ, Morrison JK (1988) Fish infected with Sphaerospora spp. Thelohan (Myxosporea) from waters enzootic for proliferative kidney disease of salmonid fish. J Protozool 35:13–18

    CAS  PubMed  Google Scholar 

  • Hedrick RP, MacConnell, De Kinkelin P (1993) Proliferative kidney disease of salmonid fish. Annu Rev Fish Dis 3:277–290

    Article  Google Scholar 

  • Kent ML, Hedrick RP (1985) PKX the causative agent of proliferative kidney disease (PKD) in pacific salmon fishes and its affinities with the Myxozoa. J Protozool 32:254–260

    CAS  PubMed  Google Scholar 

  • Kent ML, Hedrick RP (1986) Development of the PKX myxosporean in rainbow trout Salmo gairdneri. Dis Aquat Org 1:169–182

    Google Scholar 

  • Kent ML, Margolis L, Corliss JO (1994) The demise of a class of protists: taxonomic and nomenclatural revisions proposed for the protist phylum Myxozoa Grasse, 1970. Can J Zool 72:932–937

    Google Scholar 

  • Kent ML, Khattra J, Hervio DML, Devlin RH (1998) Ribosomal DNA sequence analysis of isolates of the PKX myxosporean and their relationship to members of the genus Sphaerospora. J Aquat Anim Health 10:12–21

    Google Scholar 

  • Kent ML, Khattra J, Hedrick RP, Devlin RH (2000) Tetracapsula renicola n. sp. (Myxozoa: Saccosporidae); the PKX myxozoan—the cause of proliferative kidney disease of salmonid fishes. J Parasitol 86:103–111

    CAS  PubMed  Google Scholar 

  • Longshaw M, Feist SW, Canning EU, Okamura B (1999) First identification of PKX in bryozoans from the United Kingdom—molecular evidence. Bull Eur Assoc Fish Pathol 19:146–148

    Google Scholar 

  • Longshaw M, Le Deuff R-M, Harris AF, Feist SW (2002) Development of proliferative kidney disease in rainbow trout, Oncorhynchus mykiss (Walbaum), following short-term exposure to Tetracapsula bryosalmonae infected bryozoans. J Fish Dis 25:443–449

    Article  Google Scholar 

  • Marin de Mateo M, Adams A, Richards RH, Castagnaro M, Hedrick RP (1993) Monoclonal antibody and lectin probes recognise developmental and sporogonic stages of PKX, the causative agent of proliferative kidney disease in European and North American salmonid fish. Dis Aquat Org 15:23–29

    Google Scholar 

  • Monteiro AS, Holland PWH, Okamura B (2002) Orphan worm finds a home: Buddenbrockia is a myxozoan. Mol Biol Evol 19:968–971

    CAS  PubMed  Google Scholar 

  • Morris DJ, Adams A (2002) PCR and in situ hybridization of Tetracapsula bryosalmonae (PKX), the causative agent of proliferative kidney disease. In: Cunningham CO (ed) Molecular diagnosis of salmonid diseases. Kluwer, Dordrecht, pp 299–313

  • Morris DJ, Adams A, Richards RH (2000a) Observations on the electron–dense bodies of the PKX parasite, agent of proliferative kidney disease in salmonids. Dis Aquat Org 39:201–209

    CAS  PubMed  Google Scholar 

  • Morris DJ, Adams A, Feist SW, McGeorge J, Richards RH (2000b) Immunohistochemical and PCR studies of wild fish for Tetracapsula bryosalmonae (PKX), the causative organism of proliferative kidney disease. J Fish Dis 23:129–135

    Article  Google Scholar 

  • Morris DJ, Morris DC, Adams A (2002a) Development and release of a malacosporean(Myxozoa) from Plumatella repens (Bryozoa: Phylactolaemata). Folia Parasitol 49:25–34

    PubMed  Google Scholar 

  • Morris DC, Morris DJ, Adams A (2002b) Molecular evidence of release of Tetracapsula bryosalmonae, the causative organism of proliferative kidney disease from infected salmonids into the environment. J Fish Dis 25:501–504

    Article  Google Scholar 

  • Okamura B (1996) Occurrence, prevalence, and effects of the myxozoan Tetracapsula bryozoides parasitic in the freshwater bryozoan Cristatella mucedo (Bryozoa: Phylactolaemata). Folia Parasitol 43:262–266

    Google Scholar 

  • Okamura B, Wood TS (2002) Bryozoans as hosts for Tetracapsula bryosalmonae, the PKX organism. J Fish Dis 25:469–475

    Article  Google Scholar 

  • Okamura B, Curry A, Wood TS, Canning EU (2002) Ultrastructure of Buddenbrockia identifies it as a myxozoan and verifies the bilateral origin of the Myxozoa. Parasitology 124:215–223.

    Article  CAS  PubMed  Google Scholar 

  • Rafferty MD, Mulcahy MF (1988) Is P.K.’X’ related to Sphaerospora. Bull Eur Assoc Fish Pathol 8:47

    Google Scholar 

  • Saulnier D, De Kinkelin P (1996) Antigenic and biochemical study of PKX, the myxosporean causative agent of proliferative kidney disease of salmonid fish. Dis Aquat Org 27:103–114

    CAS  Google Scholar 

  • Saulnier D, Philippe H, De Kinkelin P (1999) Molecular evidence that the proliferative kidney disease organism unknown (PKX) is a myxosporean. Dis Aquat Org 36:209–212

    CAS  PubMed  Google Scholar 

  • Seagrave CP, Bucke D, Alderman DJ (1980) Ultrastructure of a haplosporean–like organism: the possible causative agent of proliferative kidney disease in rainbow trout. J Fish Biol 16:453–459

    Google Scholar 

Download references

Acknowledgements

We thank Katherine Beauchamp and Karl B. Andree for designing the primers for the DNA probe for conducting PCR assays. We also thank William Cox from the California Department of Fish and Game and Denise Blanc of INRA, the Unité de Nutrition des Poissons, 64310 Saint-Pée-sur- Nivelle, France for their assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R.P. Hedrick.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hedrick, R., Baxa, D., De Kinkelin, P. et al. Malacosporean-like spores in urine of rainbow trout react with antibody and DNA probes to Tetracapsuloides bryosalmonae . Parasitol Res 92, 81–88 (2004). https://doi.org/10.1007/s00436-003-0986-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-003-0986-3

Keywords

Navigation